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Early puppy socialization classes: Weighing the risks vs. benefits
The American Veterinary Society of Animal Behavior (AVSAB) recently released a position paper outlining the importance of early puppy socialization, preferably before the puppy reaches 12 to 16 weeks old. Four veterinarians with extensive experience discuss early puppy socialization in a roundtable format.

Dec 1, 2009
VETERINARY MEDICINE
The American Veterinary Society of Animal Behavior (AVSAB) recently released a position paper (AVSABonline.org) outlining the importance of early puppy socialization, preferably before the puppy reaches 12 to 16 weeks old. The AVSAB encourages owners to take their pets to puppy classes as early as possible, even before puppies have completed their full vaccination series.

Some veterinarians remain concerned about allowing puppies to commingle before vaccinations are complete. So to further explore the practical and theoretical issues involved, the AVSAB has interviewed four veterinarians who have extensive experience with early puppy socialization. The participants' individual interviews are presented below in a roundtable format.
UNDERSTANDING THE BENEFITS
Dr. E. Kathryn Meyer
Dr. E. Kathryn Meyer: Let's jump right into our discussion. Some veterinarians worry about the risks of allowing puppies to interact before they have completed their full vaccination series. Let's explore our views on the risks versus the benefits of puppy classes.
Dr. Kersti Seksel: Well-run puppy classes undoubtedly provide the basis for happy, healthy dogs and happy owners. The risks of a puppy's exposure to infectious agents always need to be considered, but the risk of being euthanized or surrendered is much greater in unsocialized, untrained dogs than the risk of dying from infectious diseases.
Dr. Brenda Griffin: For puppies, the single most important part of a behavioral wellness program is proper socialization during their critical developmental period, which ends by 16 weeks. Owners must begin socialization the day they bring their new puppies home, and the clock is ticking.

Proper socialization combined with positive reinforcement-based training in the context of a group puppy class helps puppies grow into well-adjusted pets. Classes provide critical socialization time with a variety of people and other puppies. And studies clearly demonstrate that when owners invest in training classes, they are much more likely to keep their pets.1,2 The experience helps owners develop a strong bond with their pets as well as establish realistic expectations of their pets' behavior while learning proper techniques to shape it. And it's fun.
Dr. Ian Dunbar: The risks associated with attending puppy classes are minimal to nonexistent and the benefits are positively huge: Puppies learn 1) bite inhibition through puppy play and 2) proper interaction with people during off-leash play and while being handled by strangers. And owners learn to train their puppies in a controlled setting in which training is integrated with play. In this setting, a puppy's reward for training is play with other dogs.
Dr. Jennifer Messer: Relatively few risks and enormous benefits exist in allowing puppies to interact in a well-run puppy class before they've completed their vaccination series.

Canine parvovirus transmission is the main risk, as the other infectious agents we vaccinate against are either comparatively rare in prevalence and the vaccines are highly effective, or the agents cause relatively minor illness in otherwise healthy puppies. That said, even with the improved efficacy of parvovirus vaccine technology developed in the mid-1990s, about 2% to 8% of puppies may not be adequately protected from parvovirus until after they have been vaccinated at 14 to 16 weeks old.3 This percentage is relatively small, but it can't be ignored, and it must be balanced against the serious behavioral risks of holding puppies back from class until they are fully vaccinated. Specifically, poorly socialized puppies are at greater risk of behavior problems such as fear and aggression toward other dogs and people, and of being unable to engage in safe, ritualized fighting where they inhibit the force of their bite. Puppy class not only offers an opportunity for critical socialization, but is also a great forum for owners to help prevent other types of behavior problems such as housesoiling and hyperactivity (the two most commonly reported behavior problems of relinquished dogs)4 and to develop more realistic expectations of their dog—both of which play key roles in reducing the chance of relinquishment.2

Nothing we do as veterinarians is risk-free. And we routinely make medical and surgical recommendations that carry much higher risks than that of infectious disease transmission in puppy class. A good example is the up to 20% chance that hormone-responsive urinary incontinence will occur at some point after ovariohysterectomy.5 And we often make these recommendations without even discussing associated risks with clients because we think the benefits grossly outweigh any downside. Vaccine administration in general is another good example of a procedure that we carry out with little to no discussion of risks to the dog, and which carries a much higher risk of deleterious medical consequences than that of infectious disease transmission in puppy class.

Given the fact that behavior problems are the No. 1 cause of relinquishment to shelters,4 along with the fact that 56% of dogs that enter shelters in the United States are euthanized,6 and that puppy classes help prevent behavior problems and increase the likelihood of retention in the home, there must be evidence of phenomenal risk of infectious disease transmission associated with early socialization classes to warrant holding puppies back. And there is no such evidence to date. In fact, renowned behaviorist Dr. R. K. Anderson, a longtime advocate for early socialization, has more than a decade of experience and data supporting the relative safety and lack of disease transmission in puppy socialization classes in many parts of the United States.7

It's unfortunate that the behavioral gains from puppy class are under such tight age constraints. The most sound advice we can give clients is to acknowledge the small risk of infectious disease transmission and recommend well-run puppy socialization classes on the grounds that the relative risk is so low. Puppies, owners, and society stand to benefit enormously at the cost of a relatively small risk of exposure to a treatable infection.
Dr. Brenda Griffin
Dr. Ian Dunbar
Dr. Griffin: Lack of proper socialization can lead to fearfulness and the inability to cope with environmental change. Pets may be unable to habituate, especially in novel environments, and may display fear aggression. This can make them more difficult to handle for owners and veterinarians alike, and also make them more likely to be relinquished to shelters.
Severely under-socialized dogs often remain fearful for life, suffering from generalized anxiety, and are generally not suitable as pets.

Studies show that 40% of relinquished dogs have at least one problem behavior. Of those relinquished, two of the top three classes of behaviors included aggression and destructiveness. Both of these classes of behavior are sometimes associated with or motivated by fear and anxiety that result from improper socialization. 8,9
MANDATING A HEALTHY POPULATION

Dr. Meyer: What are the requirements for participating in your puppy classes?

Dr. Seksel
: Initial vaccinations must have been administered at least one week before classes start as recommended by the manufacturer and per local conditions. Because the socialization period in dogs is between 3 and 12 weeks old, I recommend that puppies be at least 8 weeks and preferably less than 13 weeks of age when they begin classes. Classes run for four or five weeks, so a puppy that is 16 weeks when it starts will be 20 to 21 weeks old when it finishes. Juvenile puppies (4 to 6 months of age) have very different mental and motor skills than younger puppies. We want them in a class with pups their own age.

Dr. Griffin: I recommend that puppies start class as soon as possible, ideally between 8 and 12 weeks old. The puppies should be receiving their distemper-hepatitis-parvovirus vaccinations, and vaccination against bordetellosis and parainfluenza is recommended. I also recommend deworming according to the Companion Animal Parasite Council guidelines.

Generally, the first class meeting would just be for the owners, who should be given basic information on housetraining, collars, leashes, positive reinforcement, socialization, and how to start training at home. We would also verify vaccination records and cover class rules. Owners are not allowed to bring their puppies to class if the pets have any signs of illness.

Depending on the puppy's origin, we may take other precautions. For example, if the pup came from a high-risk shelter environment where parvovirus infections are known to be common, we may keep the puppy out for two weeks since viruses may be shed before clinical signs appear. These owners can attend classes without their puppies. In the meantime, if these puppies are not showing signs of illness, they can still be exposed to older, vaccinated dogs and a variety of people and other reasonable novel stimuli to ensure proper socialization.

Dr. Dunbar: We require puppies to be between 10 and 18 weeks of age and to have had two distemper combination vaccines administered after 7 weeks, with the second one at least one week before class. Thus, to start class at 10 weeks of age, a puppy must have had vaccinations at 7 and 9 weeks. Deworming is encouraged but not required.

Keep in mind that socialization is an ongoing process. Breeders must never forget that by 8 weeks, the sensitive period of socialization is two-thirds over, and they must expose the puppies to a variety of people before adoption. Likewise, owners need to introduce their young puppies to people in their homes. We also encourage owners to participate in additional training classes after they've completed the first course. To remain socialized, we recommend that adolescent dogs continue to meet and interact with at least three unfamiliar people and three unfamiliar dogs a day until they are 3 years old.
Dr. Messer: All puppies attending our classes must be at least 8 weeks old. They must have had at least one distemper combination vaccination administered by a veterinarian at 6 weeks of age or older and at least 10 days before the first class. Instructors verify the vaccination record at the start of the session, and all owners are required to commit to completing their puppies' vaccination series as recommended by their veterinarians.
We recommend but do not require deworming and vaccination against kennel cough. Owners are clearly instructed to not bring a puppy to class if the puppy is sick and especially if there is any vomiting or diarrhea, unless the puppy is deemed free of infectious disease by its veterinarian.
MANAGING ON-SITE RISKS

Dr. Meyer
: All of you have basic health protocols designed to protect puppies. Do you take any other precautions?

Dr. Griffin: If an animal shelter is known to have frequent cases of parvovirus infection, which is not uncommon in the southeastern United States, we don't advise holding puppy classes on the shelter grounds. Parvovirus can survive in soil for months to years.

I prefer holding classes indoors. If an animal eliminates, the area can be thoroughly cleaned and disinfected with a 1:30 bleach-water solution. In addition, just use common sense, wash your hands, and don't bring sick puppies to class. Owners should report any illness to the pup's veterinarian and class instructor immediately.

When pups appear healthy and are vaccinated and dewormed, and when classes are conducted in a clean environment, the risk of contracting an infectious disease is extremely low.

Dr. Messer: We take many precautions. Puppy classes are held indoors and conducted before adult classes each evening. The floor is sanitized with a 1:30 bleach solution at the end of the night. We only teach on nonporous surfaces we can sanitize. Owners may help clean up urine during class, but only instructors are permitted to clean up feces. Any fecal matter deposited in class is cleaned in two stages: First a paper towel is used to remove all visible fecal matter, and then the area is disinfected with bleach solution. Instructors must either wear gloves or wash their hands thoroughly afterward.

We are in a university city with a veterinary college. So the level of pet care is quite good, and parvovirus infection is rare. If we were in a higher-risk area, we might consider removing shoes at the door, asking owners to carry their puppies from the car to the classroom, and asking that owners not walk their puppies on public property the day of class to further reduce risk.

Dr. Seksel: Ideally, puppy classes are run in a veterinary hospital so the disease status is known and problems can be effectively managed. And the veterinarian or veterinary technician can health-check puppies before each class. Floors are always appropriately cleaned and all people handling the puppies should wash their hands beforehand.

Dr. Dunbar: All of our 25 indoor facilities have impermeable, easy-to-clean floors. Any urine or fecal deposits are cleaned up immediately, and the area is heavily bleached. We ask owners to remove puppies from the course if they have bloody diarrhea or a cough.

AVOIDING EXTERNAL RISKS

Dr. Meyer:
A lot of effort goes into keeping the environment clean to minimize the potential spread of infectious disease. What recommendations do you make to puppy owners to safeguard their pets outside of puppy class?

Dr. Griffin
: Regional differences may exist, but I generally don't like dog parks for young puppies. Behavioral risks—especially injuries from rough play, dog fights, or other sensitizing stimuli that can result in generalized fear responses or aggression— associated with dog parks are present as much if not more than health risks for young pups. I prefer that puppies socialize in class with puppies of the same age group and with familiar, gentle, dog-friendly dogs that belong to friends and neighbors. Depending on a dog's temperament and size, 4 to 5 months of age (after completion of puppyhood vaccines) might be a more appropriate age to start attending dog parks—and with close supervision.

Dr. Messer: We advise owners to avoid areas heavily trafficked by dogs of unknown health and vaccination status until their puppies have had at least two distemper-hepatitis-parvovirus-parainfluenza virus vaccinations over the age of 8 weeks. If we were located in a less-affluent, higher-risk area, we might advise waiting until a puppy is at least 14 to 16 weeks old before venturing on busy public grounds. Other means of socialization during this period are encouraged, including socialization with adult dogs known to be healthy and have a current vaccination status and in areas not frequented by unknown dogs, car rides that comprise a wide range of sights and sounds, and exposure to many different people in safe settings.

Dr. Dunbar: We advise owners of very young puppies to continue socializing their pets with people in the safety of their own homes, with the precaution that outdoor shoes remain outside to reduce exposure to fomites. We also tell these owners to avoid high-risk areas, especially sidewalks and parking lots outside veterinary clinics and veterinary clinic waiting room floors. Because of the moderate year-round temperatures in our area, an owner can keep a puppy in the car until the examination time and carry the pet straight to the examination table without placing it on the ground. We also recommend avoiding dog parks and sidewalks until a puppy is 4 months old.
Dr. Jennifer Messer
Dr. Kersti Seksel
Dr. Seksel: Safeguarding puppies outside of class depends on the specific area that the puppies came from and the areas in which they now live, as disease risk is regional. The usual precautions include keeping puppies away from areas that stray dogs frequent and avoiding dog parks until the vaccination series is complete. However, it is not only the physical health that is important but also the emotional health.
We should encourage puppy owners to socialize and habituate their pets to the sights, sounds, and smells of the dog's environment in a nonthreatening manner. Puppies should not be overexposed to stimuli in their environment, such as trying to introduce them to as many substrates (e.g. corrugated surfaces, slippery surfaces) as possible or exposing them to too many activities (e.g. tunnels, teeter-totters); just because a little exposure is good does not make a lot of exposure better. Also, choosing the puppy's playmate is important. Badly behaved puppies and adult dogs can affect a puppy's behavioral responses to other dogs. For example, if a confident puppy is only exposed to confident, boisterous dogs, the puppy may not learn how to interact in a polite manner with a more timid or withdrawn puppy or dog. It may not learn how to approach slowly and sniff instead of rush over and bounce on other dogs. Therefore, all interactions with other pups need to be carefully managed in puppy classes as well as out in the wider community.
DISEASE TRANSMISSION IN CLASS

Dr. Meyer: We all know that even with precautions, there are no guarantees. Please comment on the health of the puppies taking your classes. Have any of the puppies become ill, or have you had reason to believe infectious diseases may have been spread as a consequence of the class?

Dr. Messer
: In the 13 years I have helped run puppy classes for thousands of dogs and the four years of clinical practice running puppy parenting sessions for hundreds of dogs, I have not known of any case of disease spread that could have been associated with their class attendance.

North American puppy class instructors are very concerned about the risk of disease transmission in class, both for the puppies' sake and for maintaining the veterinary community's trust—no one wants a parvovirus outbreak in class. I have not heard of cases of disease exposure or transmission in puppy classes, despite the steady trend toward decreasing the minimum age and vaccination requirements over the past 15 years.

Puppy class in itself is a progressive arm of the dog-training field, and most genuine puppy classes—classes that emphasize socialization with off-leash play and are restricted to puppies under 18 weeks of age—tend to be run by conscientious, well-informed members of the dog-training community.

Dr. Dunbar: We have occasionally had puppies become sick because of parvovirus infection while enrolled in our classes, but in over 27 years of classes we have never had a parvovirus outbreak where the infection has spread among puppies in the same class, and despite occasional parvovirus outbreaks occurring in the community. We have had kennel cough outbreaks in class, but always at a time when there has been a kennel cough outbreak in the community.

Dr. Seksel: I have never seen a disease spread because of attendance at my puppy classes. A puppy may occasionally have a bout of diarrhea or fleas, but these incidents have been unrelated to class attendance.

Dr. Griffin: I have never seen a puppy develop a life-threatening infection that was associated with attending puppy class.

CONCLUSION

Dr. Meyer: Clearly, the preponderance of evidence and practical experience support the early socialization of puppies through properly run puppy classes. Our expert panel unanimously agrees that the benefits of early socialization far outweigh the risks of infectious disease spread as long as basic precautionary strategies are in place.
Roundtable Panel

Moderator

E. Kathryn Meyer, VMD
President, American Veterinary Society of Animal Behavior, Gaithersburg, Md.

Participants

Ian Dunbar, PhD, BSc, BVetMed, MRCVS
Director, Center for Applied Animal Behavior, Berkeley, Calif.

Brenda Griffin, DVM, MS, DACVIM (small animal internal medicine)
Adjunct Associate Professor Department of Small Animal Clinical Sciences College of Veterinary Medicine, University of Florida, Gainesville, Fla.

Kersti Seksel, BVSc (Hons), MA (Hons) MRCVS, FACVSc, DACVB, DECVBM-CA
Managing Director, Sydney Animal Behaviour Service, Sydney, Australia

Jennifer Messer, BA (Hons) Psych, DVM
Director, City of Ottawa Spay and Neuter Clinic, Ontario, Canada

REFERENCES

1. Duxbury MM, Jackson JA, Line SW, et al. Evaluation of association between retention in the home and attendance at puppy socialization classes. J Am Vet Med Assoc 2003;223(1):61-66.

2. Patronek GJ, Glickman LT, Beck AM, et al. Risk factors for relinquishment of dogs to an animal shelter. J Am Vet Med Assoc 1996;209:572–581.

3. Schultz R, School of Veterinary Medicine, University of Wisconsin, Madison, Wi: Personal communication, 2008.

4. Miller DD, Staats SR, Partio C, et al. Factors associated with the decision to surrender a pet to an animal shelter. J Am Vet Med Assoc 1996:209(4):738-742.

5. Root Kustritz MV. Determining the optimal age for gonadectomy in dogs and cats. J Am Vet Med Assoc 2007;231(11):1665-1675.

6. American Humane. The about us newsroom fact sheets page. Animal shelter euthanasia. Available at: www.americanhumane.org/about-us/newsroom/fact-sheets/animal-shelter-euthanasia.html. Accessed Nov 24, 2009.

7. Animal Behavior Resources Institute, Inc. Puppy vaccination and early socialization should go together. Available at: http://abrionline.org/article.php?id=75|~http://abrionline.org/article.php?id=75/ . Accessed Nov 24, 2009.

8. Salman MD, New JG Jr, Scarlett JM, et al. Human and animal factors related to the relinquishment of dogs and cats in 12 selected animal shelters in the United States. J Appl Anim Welf Sci 1998;1(3):207-226.

9. Salman MD, Hutchinson J, Ruch-Gallie R, et al. Behavioral reasons for relinquishment of dogs and cats to 12 shelters. J Appl Anim Welf Sci 2000; 3(2):93-106.
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